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Walking naturally after spinal cord injury using a brain-spine interface.

ABSTRACT: A spinal cord injury interrupts the communication between the brain and the region of the spinal cord that produces walking, leading to paralysis^1,2. Here, we restored this communication with a digital bridge between the brain and spinal cord that enabled an individual with chronic tetraplegia to stand and walk naturally in community settings. This brain-spine interface (BSI) consists of fully implanted recording and stimulation systems that establish a direct link between cortical signals³ and the analogue modulation of epidural electrical stimulation targeting the spinal cord regions involved in the production of walking^4-6. A highly reliable BSI is calibrated within a few minutes. This reliability has remained stable over one year, including during independent use at home. The participant reports that the BSI enables natural control over the movements of his legs to stand, walk, climb stairs and even traverse complex terrains. Moreover, neurorehabilitation supported by the BSI improved neurological recovery. The participant regained the ability to walk with crutches overground even when the BSI was switched off. This digital bridge establishes a framework to restore natural control of movement after paralysis.

SUBMITTER: Lorach H

PROVIDER: S-EPMC10232367 | biostudies-literature | 2023 Jun

REPOSITORIES: biostudies-literature

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Walking naturally after spinal cord injury using a brain-spine interface.

Lorach Henri H Galvez Andrea A Spagnolo Valeria V Martel Felix F Karakas Serpil S Intering Nadine N Vat Molywan M Faivre Olivier O Harte Cathal C Komi Salif S Ravier Jimmy J Collin Thibault T Coquoz Laure L Sakr Icare I Baaklini Edeny E Hernandez-Charpak Sergio Daniel SD Dumont Gregory G Buschman Rik R Buse Nicholas N Denison Tim T van Nes Ilse I Asboth Leonie L Watrin Anne A Struber Lucas L Sauter-Starace Fabien F Langar Lilia L Auboiroux Vincent V Carda Stefano S Chabardes Stephan S Aksenova Tetiana T Demesmaeker Robin R Charvet Guillaume G Bloch Jocelyne J Courtine Grégoire G

Nature 20230524 7963

A spinal cord injury interrupts the communication between the brain and the region of the spinal cord that produces walking, leading to paralysis<sup>1,2</sup>. Here, we restored this communication with a digital bridge between the brain and spinal cord that enabled an individual with chronic tetraplegia to stand and walk naturally in community settings. This brain-spine interface (BSI) consists of fully implanted recording and stimulation systems that establish a direct link between cortical si ...[more]

PMID: 37225984

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Project description:Spinal cord injury disrupts the communication between the brain and the spinal circuits that orchestrate movement. To bypass the lesion, brain-computer interfaces have directly linked cortical activity to electrical stimulation of muscles, and have thus restored grasping abilities after hand paralysis. Theoretically, this strategy could also restore control over leg muscle activity for walking. However, replicating the complex sequence of individual muscle activation patterns underlying natural and adaptive locomotor movements poses formidable conceptual and technological challenges. Recently, it was shown in rats that epidural electrical stimulation of the lumbar spinal cord can reproduce the natural activation of synergistic muscle groups producing locomotion. Here we interface leg motor cortex activity with epidural electrical stimulation protocols to establish a brain-spine interface that alleviated gait deficits after a spinal cord injury in non-human primates. Rhesus monkeys (Macaca mulatta) were implanted with an intracortical microelectrode array in the leg area of the motor cortex and with a spinal cord stimulation system composed of a spatially selective epidural implant and a pulse generator with real-time triggering capabilities. We designed and implemented wireless control systems that linked online neural decoding of extension and flexion motor states with stimulation protocols promoting these movements. These systems allowed the monkeys to behave freely without any restrictions or constraining tethered electronics. After validation of the brain-spine interface in intact (uninjured) monkeys, we performed a unilateral corticospinal tract lesion at the thoracic level. As early as six days post-injury and without prior training of the monkeys, the brain-spine interface restored weight-bearing locomotion of the paralysed leg on a treadmill and overground. The implantable components integrated in the brain-spine interface have all been approved for investigational applications in similar human research, suggesting a practical translational pathway for proof-of-concept studies in people with spinal cord injury.

Project description:BackgroundSpinal cord injury (SCI) can leave the affected individuals with paraparesis or paraplegia, thus rendering them unable to ambulate. Since there are currently no restorative treatments for this population, novel approaches such as brain-controlled prostheses have been sought. Our recent studies show that a brain-computer interface (BCI) can be used to control ambulation within a virtual reality environment (VRE), suggesting that a BCI-controlled lower extremity prosthesis for ambulation may be feasible. However, the operability of our BCI has not yet been tested in a SCI population.MethodsFive participants with paraplegia or tetraplegia due to SCI underwent a 10-min training session in which they alternated between kinesthetic motor imagery (KMI) of idling and walking while their electroencephalogram (EEG) were recorded. Participants then performed a goal-oriented online task, where they utilized KMI to control the linear ambulation of an avatar while making 10 sequential stops at designated points within the VRE. Multiple online trials were performed in a single day, and this procedure was repeated across 5 experimental days.ResultsClassification accuracy of idling and walking was estimated offline and ranged from 60.5% (p?=?0.0176) to 92.3% (p?=?1.36×10-20) across participants and days. Offline analysis revealed that the activation of mid-frontal areas mostly in the ? and low ? bands was the most consistent feature for differentiating between idling and walking KMI. In the online task, participants achieved an average performance of 7.4±2.3 successful stops in 273±51 sec. These performances were purposeful, i.e. significantly different from the random walk Monte Carlo simulations (p<0.01), and all but one participant achieved purposeful control within the first day of the experiments. Finally, all participants were able to maintain purposeful control throughout the study, and their online performances improved over time.ConclusionsThe results of this study demonstrate that SCI participants can purposefully operate a self-paced BCI walking simulator to complete a goal-oriented ambulation task. The operation of the proposed BCI system requires short training, is intuitive, and robust against participant-to-participant and day-to-day neurophysiological variations. These findings indicate that BCI-controlled lower extremity prostheses for gait rehabilitation or restoration after SCI may be feasible in the future.

Project description:The closed-loop control of rehabilitative technologies by neural commands has shown a great potential to improve motor recovery in patients suffering from paralysis. Brain-machine interfaces (BMI) can be used as a natural control method for such technologies. BMI provides a continuous association between the brain activity and peripheral stimulation, with the potential to induce plastic changes in the nervous system. Paraplegic patients, and especially the ones with incomplete injuries, constitute a potential target population to be rehabilitated with brain-controlled robotic systems, as they may improve their gait function after the reinforcement of their spared intact neural pathways. This paper proposes a closed-loop BMI system to control an ambulatory exoskeleton-without any weight or balance support-for gait rehabilitation of incomplete spinal cord injury (SCI) patients. The integrated system was validated with three healthy subjects, and its viability in a clinical scenario was tested with four SCI patients. Using a cue-guided paradigm, the electroencephalographic signals of the subjects were used to decode their gait intention and to trigger the movements of the exoskeleton. We designed a protocol with a special emphasis on safety, as patients with poor balance were required to stand and walk. We continuously monitored their fatigue and exertion level, and conducted usability and user-satisfaction tests after the experiments. The results show that, for the three healthy subjects, 84.44 ± 14.56% of the trials were correctly decoded. Three out of four patients performed at least one successful BMI session, with an average performance of 77.6 1 ± 14.72%. The shared control strategy implemented (i.e., the exoskeleton could only move during specific periods of time) was effective in preventing unexpected movements during periods in which patients were asked to relax. On average, 55.22 ± 16.69% and 40.45 ± 16.98% of the trials (for healthy subjects and patients, respectively) would have suffered from unexpected activations (i.e., false positives) without the proposed control strategy. All the patients showed low exertion and fatigue levels during the performance of the experiments. This paper constitutes a proof-of-concept study to validate the feasibility of a BMI to control an ambulatory exoskeleton by patients with incomplete paraplegia (i.e., patients with good prognosis for gait rehabilitation).

Project description:ObjectiveThe Standing and Walking Assessment Tool (SWAT) standardizes the timing and content of walking assessments during inpatient rehabilitation by combining 12 stages ranging from lowest to highest function (0, 0.5, 1A, 1B, 1C, 2A, 2B, 2C, 3A, 3B, 3C, and 4) with 5 standard measures: the Berg Balance Scale, the modified Timed "Up & Go" test, the Activities-specific Balance Confidence Scale, the modified 6-Minute Walk Test, and the 10-Meter Walk Test (10MWT). This study aimed to determine if the SWAT at rehabilitation discharge could predict outdoor walking capacity 1-year after discharge in people with traumatic spinal cord injury.MethodsThis retrospective study used data obtained from the Rick Hansen Spinal Cord Injury Registry from 2014 to 2020. Community outdoor walking capacity was measured using the Spinal Cord Independence Measure III (SCIM III) outdoor mobility score obtained 12 (±4) months after discharge. Of 206 study participants, 90 were community nonwalkers (ie, SCIM III score 0-3), 41 were community walkers with aids (ie, SCIM III score 4-6), and 75 were independent community walkers (ie, SCIM III score 7-8). Bivariate, multivariable regression, and an area under the receiver operating characteristic curve analyses were performed.ResultsAt rehabilitation discharge, 3 significant SWAT associations were confirmed: 0-3A with community nonwalkers, 3B/higher with community walkers with and without an aid, and 4 with independent community walkers. Moreover, at discharge, a higher (Berg Balance Scale, Activities-specific Balance Confidence Scale), faster (modified Timed "Up & Go," 10MWT), or further (10MWT) SWAT measure was significantly associated with independent community walking. Multivariable analysis indicated that all SWAT measures, except the 10MWT were significant predictors of independent community walking. Furthermore, the Activities-Specific Balance Confidence Scale had the highest area under the receiver operating characteristic score (0.91), demonstrating an excellent ability to distinguish community walkers with aids from independent community walkers.ConclusionThe SWAT stage and measures at discharge can predict community outdoor walking capacity in persons with traumatic spinal cord injury. Notably, a patient's confidence in performing activities plays an important part in achieving walking ability in the community.ImpactThe discharge SWAT is useful to optimize discharge planning.

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Walking naturally after spinal cord injury using a brain-spine interface.

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Walking naturally after spinal cord injury using a brain-spine interface.

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